A Case Study of Congenital Diaphragmatic

Aquatic Mammals 2009, 35(1), 32-35, DOI 10.1578/AM.35.1.2009.32
A Case Study of Congenital Diaphragmatic Hernia in a
Juvenile Striped Dolphin (Stenella coeruleoalba)
Ronald A. Kastelein,1 Marieke F. van Dooren,2, 3 and Dick Tibboel2
SEAMARCO (Sea Mammal Research Company), Julianalaan 46, 3843 CC Harderwijk, The Netherlands;
E-mail: [email protected]
2
Department of Pediatric Surgery, Erasmus MC Rotterdam Sophia Children’s Hospital,
Dr. Molewaterplein 60, 3015 GJ Rotterdam, The Netherlands
3
Department of Clinical Genetics, Erasmus MC Rotterdam, Westzeedijk 112, 3016 AH, Rotterdam, The Netherlands
1
Abstract
Congenital Diaphragmatic Hernia (CDH) was
observed in a stranded juvenile male striped dolphin. The 2- to 3-y-old animal had survived with
its stomachs and intestines in the thoracic cavity,
which had caused a large size difference between
its two lungs. The animal also had a relatively
small penis. The animal’s combination of anomalies was either due to a genetic syndrome or caused
by maternal exposure to toxic agents.
Key Words: striped dolphin, Stenella coeruleoalba, congenital, CDH, hernia diaphragmatica,
PCB
Introduction
Many odontocetes strand annually on the Dutch
coast, most of which are dead. However, some animals strand alive and, if found in time, are transported to a veterinary treatment center (Kastelein
et al., 1997). On 5 November 1999, a male striped
dolphin (Stenella coeruleoalba) stranded alive
on the Dutch coast. The animal died soon after
arrival at the treatment center. Necropsy revealed
congenital anatomical abnormalities such as a diaphragmatic hernia, which may have been caused
by toxins in the environment. If other researchers
find similar anatomical abnormalities in striped
dolphins, efforts to study the environmental factors might need to be intensified.
Materials and Methods
The study animal had a standard length of 159
cm, a girth at the eyes of 72 cm, a girth in front
of the pectoral fins of 85 cm, an axillary girth of
90 cm, a girth in front of the dorsal fin of 88 cm,
a girth at the anus of 47 cm, and weighed 50.2 kg.
No external abnormalities were observed. Based
on body weight, body length, and growth layer
groups of the teeth, the animal was estimated to be
a juvenile of 2 to 3 y old (Di-Méglio et al., 1996;
Willy Dabin, pers. comm.).
The dolphin was taken to a marine park in the
Netherlands for veterinary treatment and rehabilitation. During transport, he remained very stressed
(indicated by his high skin temperature and high respiration rate) despite intramuscular administration of
Diazepam (Valium). Blood analysis showed no signs
of dehydration (Hematocrit: 0.54 L/L, Hemoglobin:
11.5 mmol/L, Erythrocytes: 5.1 × 1,012/L) or infection (Leucocytes: 7.3 × 109/L). After arriving at
the treatment center and being placed in a pool, the
animal displayed many muscular cramps followed
by strong, labored respirations.
The animal died 6 h after arrival at the treatment center. The carcass was frozen immediately
after death but was later thawed so that an autopsy
could be performed.
Results
Both the stomachs and the intestines were found
to be in the thoracic cavity (Figures 1 & 2). The
intestines were 22 m long and unusually varied
in color over their length. The forestomach and
fundic stomach showed no gross abnormality. The
dislocation of the abdominal organs into the thoracic cavity organs was judged to be congenital
because the left lung was less than half the volume
of the right lung (left: 700 ml vs right: 1,600 ml;
measured by water displacement in a measuring
beaker while both lungs were deflated) (Figure 3).
The lungs showed signs of pneumonia. Also, the
dorsal opening in the left side of the diaphragm
was due to the absence of a considerable part of
the diaphragm (Figure 4). The left side of the diaphragm was approximately a third of the surface
area of the right side, and the dorsal edge of the
left side of the diaphragm was smooth, rounded,
and thick (Figure 5), not a jagged edge which
would have indicated a recent rupture.
Diaphragmatic Hernia in a Striped Dolphin
33
Figure 1. The right side of the striped dolphin (right rib cage removed) showing the intestines in the thoracic cavity;
background grid: 2 × 2 cm.
Figure 2. The right side of the striped dolphin, showing the forestomach in the thoracic cavity after the intestines were
removed; background grid: 2 × 2 cm.
The animal also had hypoplasia of the penis
(micropenis; the penis was less then 10% the size
of the penis of a normal animal of this age and
size). The heart (435 g) and kidneys (left: 250 g;
right: 240 g) showed no gross abnormalities. The
blubber thickness mid-dorsally was 13 mm, midlaterally, 12 mm, and mid-ventrally, 11 mm;
this is within the range found in healthy striped
dolphins.
Based on the normal blood parameters,
the muscular cramps and labored respirations
observed during the last hours of the animal’s
life, the varied color of the intestines, and the
limited space for the stomach and intestines, the
most likely cause of death was determined to be
Congenital Diaphragmatic Hernia (CDH, hernia
diaphragmatica), the protrusion of one or more
abdominal organs through the diaphragm into
the thoracic cavity, with left lung hypoplasia and
congestion of the intestines. The animal also had
pneumonia, but it is difficult to determine whether
this was the cause of death or a result of cramps
34
Kastelein et al.
caused by congestion of the digestive tract,
which may have made the animal inhale water.
Most stranded odontocetes have pneumonia, but
this is often a secondary effect of another illness
(Kastelein et al., 1990, 1997).
Discussion
Figure 3. The left and right lungs of the striped dolphin;
note the clear size difference. Background grid: 2 × 2 cm.
Figure 4. The congenital hole in the left side of the
diaphragm (indicated by the fore and middle fingers of
the researcher) through which the stomachs and intestines
protruded into the thoracic cavity.
Figure 5. The left and right sides of the diaphragm of the
striped dolphin; note the clear asymmetry. Background
grid: 2 × 2 cm.
It is remarkable that this animal was in such
good condition when it stranded. It must have fed
shortly before stranding, despite the fact that its
left lung was half the normal size and that after
eating a meal the full forestomach must have
reduced the volume of the left lung further. Also,
it is curious that congestion of the digestive tract
did not occur sooner. Perhaps the congestion that
led to the animal’s death was due to growth of the
internal organs. In humans with CDH, the time of
intestinal circulatory failure is also quite variable.
CDH is a severe birth defect in humans, characterized by a combination of failure in diaphragm
formation and development, unilateral or bilateral lung hypoplasia, and postnatal pulmonary
hypertension. The prevalence of CDH is about
0.3 per 1,000 births. Mortality rates vary depending on case selection, particularly in cases with
associated malformations (Torfs et al., 1992).
Although efforts have been made to understand
the pathophysiology of CDH, current understanding of the etiology in humans remains sparse. The
most common anatomical type of CDH is the
posterolateral defect or Bochdalek hernia, which
represents about 96% of the cases. In humans,
the defect in the diaphragm is predominantly unilateral and on the left side as was the case in the
striped dolphin in the present study.
In animals, spontaneous occurrence of CDH
has been reported, mostly in case reports.
Diaphragmatic defects are found in albino rats
(Andersen, 1941), rabbits (Pasquet, 1974), dogs
and cats (Wilson et al., 1971), and golden lion
tamarins (Leontopithecus rosalia). In the latter,
there is familial occurrence of ventromedial to
lateral diaphragmatic hernias (Bush et al., 1980).
However, there is also a teratogen that induces diaphragmatic hernia in rats. The herbicide nitrofen
(2,4-dichlorophenyl-p-nitrophenyl ether) induces
diaphragmatic defects of the Bochdalek type and
lung hypoplasia in the offspring when administered to a pregnant rat between the 9th and 11th
d of gestation (Costlow & Manson, 1981; Kluth
et al., 1990; Tenbrinck et al., 1990). Thus, both
environmental and genetic factors are considered
to be important in the etiology of CDH (Beurskens
et al., 2007).
Unfortunately, the tissues of the study animal
were destroyed before they could be analyzed
for the presence of toxicological agents such as
Diaphragmatic Hernia in a Striped Dolphin
polychlorinated biphenyls (PCBs) in serum or
plasma or in adipose tissue. PCBs resemble nitrofen in their mechanism of action and general formula. Exposure to PCBs may have a similar effect
on diaphragm development as exposure to nitrofen. Marine animals may be exposed to these toxic
agents and are therefore at risk of developing birth
defects.
Knowledge of the chromosomal pattern of the
dolphin would be interesting because the combination of CDH and a micropenis could have been
caused by a genetic syndrome. This combination
has also been observed in humans, sometimes in
association with a deletion of the terminal part of
the long arm of chromosome 15 (Klaassens et al.,
2005) or with other chromosomal deletion syndromes. Although a certain degree of homology
exists between human and dolphin chromosomes
(Bielec et al., 1998), it would be difficult to find
small deletions.
In conclusion, the physical abnormalities—
CDH and a micropenis—of this striped dolphin
are unique. The combination of abnormalities was
either due to a genetic syndrome or caused by
maternal exposure to toxic agents.
Acknowledgments
We thank Willy Dabin (Centre de Recherche sur
les Mammifères Marins, La Rochelle) for estimating the age of the dolphin based on growth layer
counts in the teeth, and Nancy Jennings (Dotmoth.
co.uk) for providing constructive comments on
this manuscript. Rob Triesscheijn improved the
labeling of the organs on the photographs by using
Photoshop.
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